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Yang, Ling-Ling, Zhao Jiang, Yan Li, En-Tao Wang, and Xiao-Yang Zhi. "Plasmids Related to the Symbiotic Nitrogen Fixation Are Not Only Cooperated Functionally but Also May Have Evolved over a Time Span in Family Rhizobiaceae." Genome Biology and Evolution 12, no. 11 (July 20, 2020): 2002–14. http://dx.doi.org/10.1093/gbe/evaa152.
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Abstract Rhizobia are soil bacteria capable of forming symbiotic nitrogen-fixing nodules associated with leguminous plants. In fast-growing legume-nodulating rhizobia, such as the species in the family Rhizobiaceae, the symbiotic plasmid is the main genetic basis for nitrogen-fixing symbiosis, and is susceptible to horizontal gene transfer. To further understand the symbioses evolution in Rhizobiaceae, we analyzed the pan-genome of this family based on 92 genomes of type/reference strains and reconstructed its phylogeny using a phylogenomics approach. Intriguingly, although the genetic expansion that occurred in chromosomal regions was the main reason for the high proportion of low-frequency flexible gene families in the pan-genome, gene gain events associated with accessory plasmids introduced more genes into the genomes of nitrogen-fixing species. For symbiotic plasmids, although horizontal gene transfer frequently occurred, transfer may be impeded by, such as, the host’s physical isolation and soil conditions, even among phylogenetically close species. During coevolution with leguminous hosts, the plasmid system, including accessory and symbiotic plasmids, may have evolved over a time span, and provided rhizobial species with the ability to adapt to various environmental conditions and helped them achieve nitrogen fixation. These findings provide new insights into the phylogeny of Rhizobiaceae and advance our understanding of the evolution of symbiotic nitrogen fixation.
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Velázquez, Encarna, Alvaro Peix, José Luis Zurdo-Piñiro, José Luis Palomo, Pedro F. Mateos, Raúl Rivas, Estefanía Muñoz-Adelantado, Nicolás Toro, Pablo García-Benavides, and Eustoquio Martínez-Molina. "The Coexistence of Symbiosis and Pathogenicity-Determining Genes in Rhizobium rhizogenes Strains Enables Them to Induce Nodules and Tumors or Hairy Roots in Plants." Molecular Plant-Microbe Interactions® 18, no. 12 (December 2005): 1325–32. http://dx.doi.org/10.1094/mpmi-18-1325.
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Bacteria belonging to the family Rhizobiaceae may establish beneficial or harmful relationships with plants. The legume endosymbionts contain nod and nif genes responsible for nodule formation and nitrogen fixation, respectively, whereas the pathogenic strains carry vir genes responsible for the formation of tumors or hairy roots. The symbiotic and pathogenic strains currently belong to different species of the genus Rhizobium and, until now, no strains able to establish symbiosis with legumes and also to induce tumors or hairy roots in plants have been reported. Here, we report for the first time the occurrence of two rhizobial strains (163C and ATCC11325T) belonging to Rhizobium rhizogenes able to induce hairy roots or tumors in plants and also to nodulate Phaseolus vulgaris under natural environmental conditions. Symbiotic plasmids (pSym) containing nod and nif genes and pTi- or pRi-type plasmids containing vir genes were found in these strains. The nodD and nifH genes of the strains from this study are phylogenetically related to those of Sinorhizobium strains nodulating P. vulgaris. The virA and virB4 genes from strain 163C are phylogenetically related to those of R. tumefaciens C58, whereas the same genes from strain ATCC 11325T are related to those of hairy root-inducing strains. These findings may be of high relevance for the better understanding of plant-microbe interactions and knowledge of rhizobial phylogenetic history.
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Palacios, J. M., H. Manyani, M. Martínez, A. C. Ureta, B. Brito, E. Báscones, L. Rey, J. Imperial, and T. Ruiz-Argüeso. "Genetics and biotechnology of the H2-uptake [NiFe] hydrogenase from Rhizobium leguminosarum bv. viciae, a legume endosymbiotic bacterium." Biochemical Society Transactions 33, no. 1 (February 1, 2005): 94–96. http://dx.doi.org/10.1042/bst0330094.
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A limited number of strains belonging to several genera of Rhizobiaceae are capable of expressing a hydrogenase system that allows partial or full recycling of hydrogen evolved by nitrogenase, thus increasing the energy efficiency of the nitrogen fixation process. This review is focused on the genetics and biotechnology of the hydrogenase system from Rhizobium leguminosarum bv. viciae, a frequent inhabitant of European soils capable of establishing symbiotic association with peas, lentils, vetches and other legumes.
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Menéndez, Esther, Jose David Flores-Félix, Martha Helena Ramírez-Bahena, Jose M. Igual, Paula García-Fraile, Alvaro Peix, and Encarna Velázquez. "Genome Analysis of Endobacterium cerealis, a Novel Genus and Species Isolated from Zea mays Roots in North Spain." Microorganisms 8, no. 6 (June 22, 2020): 939. http://dx.doi.org/10.3390/microorganisms8060939.
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In the present work, we analyse the genomic and phenotypic characteristics of a strain named RZME27T isolated from roots of a Zea mays plant grown in Spain. The phylogenetic analyses of 16S rRNA gene and whole genome sequences showed that the strain RZME27T clustered with the type strains of Neorhizobium galegae and Pseudorhizobium pelagicum from the family Rhizobiaceae. This family encompasses several genera establishing symbiosis with legumes, but the genes involved in nodulation and nitrogen fixation are absent in its genome. Nevertheless, genes related to plant colonization, such as those involved in motility, chemotaxis, quorum sensing, exopolysaccharide biosynthesis and hydrolytic enzymes production were found. The comparative pangenomic analyses showed that 78 protein clusters present in the strain RZME27T were not found in the type strains of its closest relatives N. galegae and P. pelagicum. The calculated average nucleotide identity (ANI) values between the strain RZME27T and the type strains of N. galegae and P. pelagicum were 75.61% and 75.1%, respectively, similar or lower than those found for other genera from family Rhizobiaceae. Several phenotypic differences were also found, highlighting the absence of the fatty acid C19:0 cyclo ω8c and propionate assimilation. These results support the definition of a novel genus and species named Endobacterium cerealis gen. nov. sp. nov. whose type strain is RZME27T.
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Crespo-Rivas, Juan, Pilar Navarro-Gómez, Cynthia Alias-Villegas, Jie Shi, Tao Zhen, Yanbo Niu, Virginia Cuéllar, et al. "Sinorhizobium fredii HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean." International Journal of Molecular Sciences 20, no. 3 (February 12, 2019): 787. http://dx.doi.org/10.3390/ijms20030787.
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Members of Rhizobiaceae contain a homologue of the iron-responsive regulatory protein RirA. In different bacteria, RirA acts as a repressor of iron uptake systems under iron-replete conditions and contributes to ameliorate cell damage during oxidative stress. In Rhizobium leguminosarum and Sinorhizobium meliloti, mutations in rirA do not impair symbiotic nitrogen fixation. In this study, a rirA mutant of broad host range S. fredii HH103 has been constructed (SVQ780) and its free-living and symbiotic phenotypes evaluated. No production of siderophores could be detected in either the wild-type or SVQ780. The rirA mutant exhibited a growth advantage under iron-deficient conditions and hypersensitivity to hydrogen peroxide in iron-rich medium. Transcription of rirA in HH103 is subject to autoregulation and inactivation of the gene upregulates fbpA, a gene putatively involved in iron transport. The S. fredii rirA mutant was able to nodulate soybean plants, but symbiotic nitrogen fixation was impaired. Nodules induced by the mutant were poorly infected compared to those induced by the wild-type. Genetic complementation reversed the mutant’s hypersensitivity to H2O2, expression of fbpA, and symbiotic deficiency in soybean plants. This is the first report that demonstrates a role for RirA in the Rhizobium-legume symbiosis.
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Kumari, Diksha, and Dipjyoti Chakraborty. "Drought stress mitigation in Vigna radiata by the application of root-nodulating bacteria." Plant Science Today 4, no. 4 (December 4, 2017): 209–12. http://dx.doi.org/10.14719/pst.2017.4.4.343.
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Plant growth promoting rhizobacteria (PGPR) facilitates plant growth and are of potential use as bio-fertilizer. Pulses are an important protein source in the vegetarian diet and being legumes harbour members of the Rhizobiaceae that form symbiotic relationships and nodules involved in nitrogen fixation. Vigna radiata is one such pulse crop popular in India. Nodulating bacteria were also found to mitigate biotic and abiotc stress and may be used as an alternative to chemical fertilizer for a sustainable agriculture. Here, we review rhizobial species isolated from V. radiata that have offered an efficient drought stress tolerance.
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Frendo, Pierre, Judith Harrison, Christel Norman, María Jesús Hernández Jiménez, Ghislaine Van de Sype, Alain Gilabert, and Alain Puppo. "Glutathione and Homoglutathione Play a Critical Role in the Nodulation Process of Medicago truncatula." Molecular Plant-Microbe Interactions® 18, no. 3 (March 2005): 254–59. http://dx.doi.org/10.1094/mpmi-18-0254.
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Legumes form a symbiotic interaction with bacteria of the Rhizobiaceae family toproduce nitrogen-fixing root nodules under nitrogen-limiting conditions. This process involves the recognition of the bacterial Nod factors by the plant which mediates the entry of the bacteria into the root and nodule organogenesis. We have examined the importance of the low molecular weight thiols, glutathione (GSH) and homoglutathione (hGSH), during the nodulation process in the model legume Medicago truncatula. Using both buthionine sulfoximine, a specific inhibitor of GSH and hGSH synthesis, and transgenic roots expressing GSH synthetase and hGSH synthetase in an antisense orientation, we showed that deficiency in GSH and hGSH synthesis inhibited the formation of the root nodules. This inhibition was not correlated to a modification in the number of infection events or to a change in the expression of the Rhizobium sp.-induced peroxidase rip1, indicating that the low level of GSH or hGSH did not alter the first steps of the infection process. In contrast, a strong diminution in the number of nascent nodules and in the expression of the early nodulin genes, Mtenod12 and Mtenod40, were observed in GSHand hGSH-depleted plants. In conclusion, GSH and hGSH appear to be essential for proper development of the root nodules during the symbiotic interaction.
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Safronova, Vera I., Polina V. Guro, Anna L. Sazanova, Irina G. Kuznetsova, Andrey A. Belimov, Valentin V. Yakubov, Elizaveta R. Chirak, et al. "Rhizobial Microsymbionts of Kamchatka Oxytropis Species Possess Genes of the Type III and VI Secretion Systems, Which Can Affect the Development of Symbiosis." Molecular Plant-Microbe Interactions® 33, no. 10 (October 2020): 1232–41. http://dx.doi.org/10.1094/mpmi-05-20-0114-r.
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A collection of rhizobial strains isolated from root nodules of the narrowly endemic legume species Oxytropis erecta, O. anadyrensis, O. kamtschatica, and O. pumilio originating from the Kamchatka Peninsula (Russian Federation) was obtained. Analysis of the 16S ribosomal RNA gene sequence showed a significant diversity of isolates belonging to families Rhizobiaceae (genus Rhizobium), Phyllobacteriaceae (genera Mesorhizobium, Phyllobacterium), and Bradyrhizobiaceae (genera Bosea, Tardiphaga). A plant nodulation assay showed that only strains belonging to genus Mesorhizobium could form nitrogen-fixing nodules on Oxytropis plants. The strains M. loti 582 and M. huakuii 583, in addition to symbiotic clusters, possessed genes of the type III and type VI secretion systems (T3SS and T6SS, respectively), which can influence the host specificity of strains. These strains formed nodules of two types (elongated and rounded) on O. kamtschatica roots. We suggest this phenomenon may result from Nod factor–dependent and –independent nodulation strategies. The obtained strains are of interest for further study of the T3SS and T6SS gene function and their role in the development of rhizobium-legume symbiosis. The prospects of using rhizobia having both gene systems related to symbiotic and nonsymbiotic nodulation strategies to enhance the efficiency of plant-microbe interactions by expanding the host specificity and increasing nodulation efficiency are discussed.
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Trevaskis, Ben, Gillian Colebatch, Guilhem Desbrosses, Maren Wandrey, Stefanie Wienkoop, Gerhard Saalbach, and Michael Udvardi. "Differentiation of Plant Cells During Symbiotic Nitrogen Fixation." Comparative and Functional Genomics 3, no. 2 (2002): 151–57. http://dx.doi.org/10.1002/cfg.155.
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Nitrogen-fixing symbioses between legumes and bacteria of the family Rhizobiaceae involve differentiation of both plant and bacterial cells. Differentiation of plant root cells is required to build an organ, the nodule, which can feed and accommodate a large population of bacteria under conditions conducive to nitrogen fixation. An efficient vascular system is built to connect the nodule to the root, which delivers sugars and other nutrients to the nodule and removes the products of nitrogen fixation for use in the rest of the plant. Cells in the outer cortex differentiate to form a barrier to oxygen diffusion into nodules, which helps to produce the micro-aerobic environment necessary for bacterial nitrogenase activity. Cells of the central, infected zone of nodules undergo multiple rounds of endoreduplication, which may be necessary for colonisation by rhizobia and may enable enlargement and greater metabolic activity of these cells. Infected cells of the nodule contain rhizobia within a unique plant membrane called the peribacteroid or symbiosome membrane, which separates the bacteria from the host cell cytoplasm and mediates nutrient and signal exchanges between the partners. Rhizobia also undergo differentiation during nodule development. Not surprisingly, perhaps, differentiation of each partner is dependent upon interactions with the other. High-throughput methods to assay gene transcripts, proteins, and metabolites are now being used to explore further the different aspects of plant and bacterial differentiation. In this review, we highlight recent advances in our understanding of plant cell differentiation during nodulation that have been made, at least in part, using high-throughput methods.
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Brencic, Anja, and Stephen C. Winans. "Detection of and Response to Signals Involved in Host-Microbe Interactions by Plant-Associated Bacteria." Microbiology and Molecular Biology Reviews 69, no. 1 (March 2005): 155–94. http://dx.doi.org/10.1128/mmbr.69.1.155-194.2005.
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SUMMARY Diverse interactions between hosts and microbes are initiated by the detection of host-released chemical signals. Detection of these signals leads to altered patterns of gene expression that culminate in specific and adaptive changes in bacterial physiology that are required for these associations. This concept was first demonstrated for the members of the family Rhizobiaceae and was later found to apply to many other plant-associated bacteria as well as to microbes that colonize human and animal hosts. The family Rhizobiaceae includes various genera of rhizobia as well as species of Agrobacterium. Rhizobia are symbionts of legumes, which fix nitrogen within root nodules, while Agrobacterium tumefaciens is a pathogen that causes crown gall tumors on a wide variety of plants. The plant-released signals that are recognized by these bacteria are low-molecular-weight, diffusible molecules and are detected by the bacteria through specific receptor proteins. Similar phenomena are observed with other plant pathogens, including Pseudomonas syringae, Ralstonia solanacearum, and Erwinia spp., although here the signals and signal receptors are not as well defined. In some cases, nutritional conditions such as iron limitation or the lack of nitrogen sources seem to provide a significant cue. While much has been learned about the process of host detection over the past 20 years, our knowledge is far from being complete. The complex nature of the plant-microbe interactions makes it extremely challenging to gain a comprehensive picture of host detection in natural environments, and thus many signals and signal recognition systems remain to be described.
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Giraud, Eric, and Darrell Fleischman. "Nitrogen-fixing symbiosis between photosynthetic bacteria and legumes." Photosynthesis Research 82, no. 2 (November 2004): 115–30. http://dx.doi.org/10.1007/s11120-004-1768-1.
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Sy, Abdoulaye, Eric Giraud, Philippe Jourand, Nelly Garcia, Anne Willems, Philippe de Lajudie, Yves Prin, et al. "Methylotrophic MethylobacteriumBacteria Nodulate and Fix Nitrogen in Symbiosis with Legumes." Journal of Bacteriology 183, no. 1 (January 1, 2001): 214–20. http://dx.doi.org/10.1128/jb.183.1.214-220.2001.
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ABSTRACT Rhizobia described so far belong to three distinct phylogenetic branches within the α-2 subclass ofProteobacteria. Here we report the discovery of a fourth rhizobial branch involving bacteria of theMethylobacterium genus. Rhizobia isolated fromCrotalaria legumes were assigned to a new species, “Methylobacterium nodulans,” within theMethylobacterium genus on the basis of 16S ribosomal DNA analyses. We demonstrated that these rhizobia facultatively grow on methanol, which is a characteristic ofMethylobacterium spp. but a unique feature among rhizobia. Genes encoding two key enzymes of methylotrophy and nodulation, the mxaF gene, encoding the α subunit of the methanol dehydrogenase, and the nodA gene, encoding an acyltransferase involved in Nod factor biosynthesis, were sequenced for the type strain, ORS2060. Plant tests and nodAamplification assays showed that “M. nodulans” is the only nodulating Methylobacterium sp. identified so far. Phylogenetic sequence analysis showed that “M. nodulans” NodA is closely related to BradyrhizobiumNodA, suggesting that this gene was acquired by horizontal gene transfer.
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Masson-Boivin, Catherine, Eric Giraud, Xavier Perret, and Jacques Batut. "Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?" Trends in Microbiology 17, no. 10 (October 2009): 458–66. http://dx.doi.org/10.1016/j.tim.2009.07.004.
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Marchetti, Marta, Alain Jauneau, Delphine Capela, Philippe Remigi, Carine Gris, Jacques Batut, and Catherine Masson-Boivin. "Shaping Bacterial Symbiosis With Legumes by Experimental Evolution." Molecular Plant-Microbe Interactions® 27, no. 9 (September 2014): 956–64. http://dx.doi.org/10.1094/mpmi-03-14-0083-r.
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Nitrogen-fixing symbionts of legumes have appeared after the emergence of legumes on earth, approximately 70 to 130 million years ago. Since then, symbiotic proficiency has spread to distant genera of α- and β-proteobacteria, via horizontal transfer of essential symbiotic genes and subsequent recipient genome remodeling under plant selection pressure. To tentatively replay rhizobium evolution in laboratory conditions, we previously transferred the symbiotic plasmid of the Mimosa symbiont Cupriavidus taiwanensis in the plant pathogen Ralstonia solanacearum, and selected spontaneous nodulating variants of the chimeric Ralstonia sp. using Mimosa pudica as a trap. Here, we pursued the evolution experiment by submitting two of the rhizobial drafts to serial ex planta–in planta (M. pudica) passages that may mimic alternating of saprophytic and symbiotic lives of rhizobia. Phenotyping 16 cycle-evolved clones showed strong and parallel evolution of several symbiotic traits (i.e., nodulation competitiveness, intracellular infection, and bacteroid persistence). Simultaneously, plant defense reactions decreased within nodules, suggesting that the expression of symbiotic competence requires the capacity to limit plant immunity. Nitrogen fixation was not acquired in the frame of this evolutionarily short experiment, likely due to the still poor persistence of final clones within nodules compared with the reference rhizobium C. taiwanensis. Our results highlight the potential of experimental evolution in improving symbiotic proficiency and for the elucidation of relationship between symbiotic capacities and elicitation of immune responses.
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Day, David A., and Penelope M. C. Smith. "Iron Transport across Symbiotic Membranes of Nitrogen-Fixing Legumes." International Journal of Molecular Sciences 22, no. 1 (January 4, 2021): 432. http://dx.doi.org/10.3390/ijms22010432.
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Iron is an essential nutrient for the legume-rhizobia symbiosis and nitrogen-fixing bacteroids within root nodules of legumes have a very high demand for the metal. Within the infected cells of nodules, the bacteroids are surrounded by a plant membrane to form an organelle-like structure called the symbiosome. In this review, we focus on how iron is transported across the symbiosome membrane and accessed by the bacteroids.
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Werner, Gijsbert D. A., William K. Cornwell, Johannes H. C. Cornelissen, and E. Toby Kiers. "Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism." Proceedings of the National Academy of Sciences 112, no. 33 (June 3, 2015): 10262–69. http://dx.doi.org/10.1073/pnas.1424030112.
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Understanding the origins and evolutionary trajectories of symbiotic partnerships remains a major challenge. Why are some symbioses lost over evolutionary time whereas others become crucial for survival? Here, we use a quantitative trait reconstruction method to characterize different evolutionary stages in the ancient symbiosis between legumes (Fabaceae) and nitrogen-fixing bacteria, asking how labile is symbiosis across different host clades. We find that more than half of the 1,195 extant nodulating legumes analyzed have a high likelihood (>95%) of being in a state of high symbiotic persistence, meaning that they show a continued capacity to form the symbiosis over evolutionary time, even though the partnership has remained facultative and is not obligate. To explore patterns associated with the likelihood of loss and retention of the N2-fixing symbiosis, we tested for correlations between symbiotic persistence and legume distribution, climate, soil and trait data. We found a strong latitudinal effect and demonstrated that low mean annual temperatures are associated with high symbiotic persistence in legumes. Although no significant correlations between soil variables and symbiotic persistence were found, nitrogen and phosphorus leaf contents were positively correlated with legumes in a state of high symbiotic persistence. This pattern suggests that highly demanding nutrient lifestyles are associated with more stable partnerships, potentially because they “lock” the hosts into symbiotic dependency. Quantitative reconstruction methods are emerging as a powerful comparative tool to study broad patterns of symbiont loss and retention across diverse partnerships.
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Bazin, Jérémie, Pilar Bustos-Sanmamed, Caroline Hartmann, Christine Lelandais-Brière, and Martin Crespi. "Complexity of miRNA-dependent regulation in root symbiosis." Philosophical Transactions of the Royal Society B: Biological Sciences 367, no. 1595 (June 5, 2012): 1570–79. http://dx.doi.org/10.1098/rstb.2011.0228.
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The development of root systems may be strongly affected by the symbiotic interactions that plants establish with soil organisms. Legumes are able to develop symbiotic relationships with both rhizobial bacteria and arbuscular mycorrhizal fungi leading to the formation of nitrogen-fixing nodules and mycorrhizal arbuscules, respectively. Both of these symbiotic interactions involve complex cellular reprogramming and profound morphological and physiological changes in specific root cells. In addition, the repression of pathogenic defence responses seems to be required for successful symbiotic interactions. Apart from typical regulatory genes, such as transcription factors, microRNAs (miRNAs) are emerging as riboregulators that control gene networks in eukaryotic cells through interactions with specific target mRNAs. In recent years, the availability of deep-sequencing technologies and the development of in silico approaches have allowed for the identification of large sets of miRNAs and their targets in legumes . A number of conserved and legume-specific miRNAs were found to be associated with symbiotic interactions as shown by their expression patterns or actions on symbiosis-related targets. In this review, we combine data from recent literature and genomic and deep-sequencing data on miRNAs controlling nodule development or restricting defence reactions to address the diversity and specificity of miRNA-dependent regulation in legume root symbiosis. Phylogenetic analysis of miRNA isoforms and their potential targets suggests a role for miRNAs in the repression of plant defence during symbiosis and revealed the evolution of miRNA-dependent regulation in legumes to allow for the modification of root cell specification, such as the formation of mycorrhized roots and nitrogen-fixing nodules.
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Singh, R. J., G. H. Chung, and R. L. Nelson. "Landmark research in legumes." Genome 50, no. 6 (June 2007): 525–37. http://dx.doi.org/10.1139/g07-037.
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Legumes are members of the family Fabaceae or Leguminosae and include economically important grain legumes, oilseed crops, forage crops, shrubs, and tropical or subtropical trees. Legumes are a rich source of quality protein for humans and animals. They also enrich the soil by producing their own nitrogen in symbiosis with nitrogen-fixing bacteria. International centers and national institutes collect, maintain, distribute, and produce high-yielding legumes (grain-pulses, oilseeds, forages, nutraceuticals, medicinal shrubs, and trees). Legume breeders are confined within the primary gene pools (GP-1) in their varietal improvement programs and have not exploited secondary gene pools (GP-2), tertiary gene pools (GP-3), or quaternary gene pools (GP-4). Legumes are also an excellent source of timber, medicine, nutraceuticals, tannins, gums, insecticides, resins, varnish, paints, dyes, and eco-friendly by-products such as soy diesel. Three forage crops, Medicago truncatula , Lotus japonicus , and Trifolium pratense , are model legumes for phylogenetic studies and genome sequencing. This paper concludes that a “protein revolution” is needed to meet the protein demands of the world.
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Sharma, Vinay, Samrat Bhattacharyya, Rakesh Kumar, Ashish Kumar, Fernando Ibañez, Jianping Wang, Baozhu Guo, et al. "Molecular Basis of Root Nodule Symbiosis between Bradyrhizobium and ‘Crack-Entry’ Legume Groundnut (Arachis hypogaea L.)." Plants 9, no. 2 (February 20, 2020): 276. http://dx.doi.org/10.3390/plants9020276.
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Nitrogen is one of the essential plant nutrients and a major factor limiting crop productivity. To meet the requirements of sustainable agriculture, there is a need to maximize biological nitrogen fixation in different crop species. Legumes are able to establish root nodule symbiosis (RNS) with nitrogen-fixing soil bacteria which are collectively called rhizobia. This mutualistic association is highly specific, and each rhizobia species/strain interacts with only a specific group of legumes, and vice versa. Nodulation involves multiple phases of interactions ranging from initial bacterial attachment and infection establishment to late nodule development, characterized by a complex molecular signalling between plants and rhizobia. Characteristically, legumes like groundnut display a bacterial invasion strategy popularly known as “crack-entry’’ mechanism, which is reported approximately in 25% of all legumes. This article accommodates critical discussions on the bacterial infection mode, dynamics of nodulation, components of symbiotic signalling pathway, and also the effects of abiotic stresses and phytohormone homeostasis related to the root nodule symbiosis of groundnut and Bradyrhizobium. These parameters can help to understand how groundnut RNS is programmed to recognize and establish symbiotic relationships with rhizobia, adjusting gene expression in response to various regulations. This review further attempts to emphasize the current understanding of advancements regarding RNS research in the groundnut and speculates on prospective improvement possibilities in addition to ways for expanding it to other crops towards achieving sustainable agriculture and overcoming environmental challenges.
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Klinger, Christie R., Jennifer A. Lau, and Katy D. Heath. "Ecological genomics of mutualism decline in nitrogen-fixing bacteria." Proceedings of the Royal Society B: Biological Sciences 283, no. 1826 (March 16, 2016): 20152563. http://dx.doi.org/10.1098/rspb.2015.2563.
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Anthropogenic changes can influence mutualism evolution; however, the genomic regions underpinning mutualism that are most affected by environmental change are generally unknown, even in well-studied model mutualisms like the interaction between legumes and their nitrogen (N)-fixing rhizobia. Such genomic information can shed light on the agents and targets of selection maintaining cooperation in nature. We recently demonstrated that N-fertilization has caused an evolutionary decline in mutualistic partner quality in the rhizobia that form symbiosis with clover. Here, population genomic analyses of N-fertilized versus control rhizobium populations indicate that evolutionary differentiation at a key symbiosis gene region on the symbiotic plasmid (pSym) contributes to partner quality decline. Moreover, patterns of genetic variation at selected loci were consistent with recent positive selection within N-fertilized environments, suggesting that N-rich environments might select for less beneficial rhizobia. By studying the molecular population genomics of a natural bacterial population within a long-term ecological field experiment, we find that: (i) the N environment is indeed a potent selective force mediating mutualism evolution in this symbiosis, (ii) natural variation in rhizobium partner quality is mediated in part by key symbiosis genes on the symbiotic plasmid, and (iii) differentiation at selected genes occurred in the context of otherwise recombining genomes, resembling eukaryotic models of adaptation.
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Vaz Martins, Teresa, and Valerie N. Livina. "What Drives Symbiotic Calcium Signalling in Legumes? Insights and Challenges of Imaging." International Journal of Molecular Sciences 20, no. 9 (May 7, 2019): 2245. http://dx.doi.org/10.3390/ijms20092245.
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We review the contribution of bioimaging in building a coherent understanding of Ca 2 + signalling during legume-bacteria symbiosis. Currently, two different calcium signals are believed to control key steps of the symbiosis: a Ca 2 + gradient at the tip of the legume root hair is involved in the development of an infection thread, while nuclear Ca 2 + oscillations, the hallmark signal of this symbiosis, control the formation of the root nodule, where bacteria fix nitrogen. Additionally, different Ca 2 + spiking signatures have been associated with specific infection stages. Bioimaging is intrinsically a cross-disciplinary area that requires integration of image recording, processing and analysis. We used experimental examples to critically evaluate previously-established conclusions and draw attention to challenges caused by the varying nature of the signal-to-noise ratio in live imaging. We hypothesise that nuclear Ca 2 + spiking is a wide-range signal involving the entire root hair and that the Ca 2 + signature may be related to cytoplasmic streaming.
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Bala, Neeru, P. K. Sharma, and K. Lakshminarayana. "Nodulation and nitrogen fixation by salinity-tolerant rhizobia in symbiosis with tree legumes." Agriculture, Ecosystems & Environment 33, no. 1 (November 1990): 33–46. http://dx.doi.org/10.1016/0167-8809(90)90142-z.
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Patriarca, Eduardo J., Rosarita Tatè, and Maurizio Iaccarino. "Key Role of Bacterial NH4+ Metabolism in Rhizobium-Plant Symbiosis." Microbiology and Molecular Biology Reviews 66, no. 2 (June 2002): 203–22. http://dx.doi.org/10.1128/mmbr.66.2.203-222.2002.
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SUMMARY Symbiotic nitrogen fixation is carried out in specialized organs, the nodules, whose formation is induced on leguminous host plants by bacteria belonging to the family Rhizobiaceae. Nodule development is a complex multistep process, which requires continued interaction between the two partners and thus the exchange of different signals and metabolites. NH4 + is not only the primary product but also the main regulator of the symbiosis: either as ammonium and after conversion into organic compounds, it regulates most stages of the interaction, from the production of nodule inducers to the growth, function, and maintenance of nodules. This review examines the adaptation of bacterial NH4 + metabolism to the variable environment generated by the plant, which actively controls and restricts bacterial growth by affecting oxygen and nutrient availability, thereby allowing a proficient interaction and at the same time preventing parasitic invasion. We describe the regulatory circuitry responsible for the downregulation of bacterial genes involved in NH4 + assimilation occurring early during nodule invasion. This is a key and necessary step for the differentiation of N2-fixing bacteroids (the endocellular symbiotic form of rhizobia) and for the development of efficient nodules.
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Barros, Felipe Martins do Rêgo, Giselle Gomes Monteiro Fracetto, Felipe José Cury Fracetto, José Petrônio Mendes Júnior, Victor Lucas Vieira Prudêncio de Araújo, and Mario Andrade Lira Junior. "Silvopastoral systems drive the nitrogen-cycling bacterial community in soil." Ciência e Agrotecnologia 42, no. 3 (June 2018): 281–90. http://dx.doi.org/10.1590/1413-70542018423031117.
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ABSTRACT Intercropping tree legumes with forage grasses in a silvopastoral system can avoid pasture degradation benefiting the soil. In such a system, nitrogen (N) is supplied by symbiosis between legumes and bacteria. However, the pasture quality determines the action of free-living nitrogen-fixing bacteria, which possess nifH genes, which encode nitrogenase enzyme. Ammonium-oxidizing bacteria (AOB), involved in the nitrification step, can be evaluated by specific regions of the 16S rRNA corresponding to AOB. Thus, we investigated the influence of the introduction of tree legumes into a silvopastoral system on the community structure and abundance of total bacteria, diazotrophic bacteria and ammonium-oxidizing bacteria by DGGE (denaturing gradient gel electrophoresis) and real-time qPCR (quantitative PCR). The experiment involved nine plots of one hectare each, planted with sabia (Mimosa caesalpinifolia), a Gliricidia species (Gliricidia sepium), and a Brachiaria species (Brachiaria decumbens) in a randomized block design, forming three treatments: I-Brachiaria intercropped with sabia; II-Brachiaria intercropped with Gliricidia and III-Brachiaria only, with three replicates. The structures of the total bacterial and ammonium-oxidizing bacterial communities were influenced by tree legume introduction, possibly through modification of the soil chemical attributes. The copy numbers of total bacteria, ammonium-oxidizing bacteria and diazotrophic bacteria were higher in soils planted with legumes, which provided better conditions for microbial growth compared to planting with the Brachiaria species alone. Silvopastoral management with tree legumes improves the biological quality of soil, favouring the bacterial community linked to N-cycling.
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Arnold, Markus F. F., Jon Penterman, Mohammed Shabab, Esther J. Chen, and Graham C. Walker. "Important Late-Stage Symbiotic Role of theSinorhizobium melilotiExopolysaccharide Succinoglycan." Journal of Bacteriology 200, no. 13 (April 9, 2018): e00665-17. http://dx.doi.org/10.1128/jb.00665-17.
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ABSTRACTSinorhizobium melilotienters into beneficial symbiotic interactions withMedicagospecies of legumes. Bacterial exopolysaccharides play critical signaling roles in infection thread initiation and growth during the early stages of root nodule formation. After endocytosis ofS. melilotiby plant cells in the developing nodule, plant-derived nodule-specific cysteine-rich (NCR) peptides mediate terminal differentiation of the bacteria into nitrogen-fixing bacteroids. Previous transcriptional studies showed that the intensively studied cationic peptide NCR247 induces expression of theexogenes that encode the proteins required for succinoglycan biosynthesis. In addition, genetic studies have shown that someexomutants exhibit increased sensitivity to the antimicrobial action of NCR247. Therefore, we investigated whether the symbiotically activeS. melilotiexopolysaccharide succinoglycan can protectS. melilotiagainst the antimicrobial activity of NCR247. We discovered that high-molecular-weight forms of succinoglycan have the ability to protectS. melilotifrom the antimicrobial action of the NCR247 peptide but low-molecular-weight forms of wild-type succinoglycan do not. The protective function of high-molecular-weight succinoglycan occurs via direct molecular interactions between anionic succinoglycan and the cationic NCR247 peptide, but this interaction is not chiral. Taken together, our observations suggest thatS. melilotiexopolysaccharides not only may be critical during early stages of nodule invasion but also are upregulated at a late stage of symbiosis to protect bacteria against the bactericidal action of cationic NCR peptides. Our findings represent an important step forward in fully understanding the complete set of exopolysaccharide functions during legume symbiosis.IMPORTANCESymbiotic interactions between rhizobia and legumes are economically important for global food production. The legume symbiosis also is a major part of the global nitrogen cycle and is an ideal model system to study host-microbe interactions. Signaling between legumes and rhizobia is essential to establish symbiosis, and understanding these signals is a major goal in the field. Exopolysaccharides are important in the symbiotic context because they are essential signaling molecules during early-stage symbiosis. In this study, we provide evidence suggesting that theSinorhizobium melilotiexopolysaccharide succinoglycan also protects the bacteria against the antimicrobial action of essential late-stage symbiosis plant peptides.
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MOREIRA, Fatima Maria de Souza, Katia Pereira COELHO, Paula Rose de Almeida RIBEIRO, and Amanda Azarias GUIMARÃES. "Nursery growth and rhizobia symbiosis of scandent Leguminosae species native to the Amazon region." Acta Amazonica 46, no. 4 (December 2016): 367–76. http://dx.doi.org/10.1590/1809-4392201600392.
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ABSTRACT A great number of species and individuals of scandent legumes establishing symbiosis with nitrogen fixing bacteria occurs in the Amazon Forest. These symbiosis probably play an important role in contributing to nitrogen incorporation in this ecossystem. The objectives of this study were to evaluate the growth of eight species of scandent legumes in five nursery substrates; to compare nodulation with rhizobia strains introduced or native to these substrates; and to characterize phenotypically and genetically these rhizobia. The experiment was carried out in a completely randomized design with five replications. Five to seven months after seedling emergency, according to the legume species, growth and nodulation parameters were determined. Rhizobia identification of strains was carried out by 16S rRNA gene partial sequencing. The survival of seedlings after the transplanting varied from 93 to 98%, in Ultisol (Argissolo in Brazilian classification), collected in primary forest, and fertilized with all nutrients, except nitrogen (ULTfert); and in a clay and sand mixture, in a ratio 3:2 (CONV), respectively. Species with height superior to 30 cm, in general, grew better in substrates with higher fertility: ULTfert and Humic Gley soil (HG). Seven out of the eight species were able to nodulate. The percentage of nodulation per substrate was: SAND, washed sand with mixed inoculum of 100 rhizobia strains plus fertilization (100), HG (80), CONV (100), ULT, A-horizon of red-yellow Ultisol collected in the Ducke Forest Reserve (Manaus) (44), and ULTfert (55%). Bradyrhizobium spp. were isolated from nodules of all species and substrates. Burkolderia fungorum was isolated from Dalbergia inundata. For Dalbergia riedelli and Dalbergia inundata, this is the first report on the identification of symbiotic strains. Scandent legumes present high survival of seedlings in nursery, and develop better in substrates with higher fertility, and generally present symbiosis with Bradyrhizobium.
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Fagorzi, Camilla, Alice Checcucci, George diCenzo, Klaudia Debiec-Andrzejewska, Lukasz Dziewit, Francesco Pini, and Alessio Mengoni. "Harnessing Rhizobia to Improve Heavy-Metal Phytoremediation by Legumes." Genes 9, no. 11 (November 8, 2018): 542. http://dx.doi.org/10.3390/genes9110542.
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Rhizobia are bacteria that can form symbiotic associations with plants of the Fabaceae family, during which they reduce atmospheric di-nitrogen to ammonia. The symbiosis between rhizobia and leguminous plants is a fundamental contributor to nitrogen cycling in natural and agricultural ecosystems. Rhizobial microsymbionts are a major reason why legumes can colonize marginal lands and nitrogen-deficient soils. Several leguminous species have been found in metal-contaminated areas, and they often harbor metal-tolerant rhizobia. In recent years, there have been numerous efforts and discoveries related to the genetic determinants of metal resistance by rhizobia, and on the effectiveness of such rhizobia to increase the metal tolerance of host plants. Here, we review the main findings on the metal resistance of rhizobia: the physiological role, evolution, and genetic determinants, and the potential to use native and genetically-manipulated rhizobia as inoculants for legumes in phytoremediation practices.
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Alloing, Geneviève, Karine Mandon, Eric Boncompagni, Françoise Montrichard, and Pierre Frendo. "Involvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia." Antioxidants 7, no. 12 (December 5, 2018): 182. http://dx.doi.org/10.3390/antiox7120182.
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Leguminous plants can form a symbiotic relationship with Rhizobium bacteria, during which plants provide bacteria with carbohydrates and an environment appropriate to their metabolism, in return for fixed atmospheric nitrogen. The symbiotic interaction leads to the formation of a new organ, the root nodule, where a coordinated differentiation of plant cells and bacteria occurs. The establishment and functioning of nitrogen-fixing symbiosis involves a redox control important for both the plant-bacteria crosstalk and the regulation of nodule metabolism. In this review, we discuss the involvement of thioredoxin and glutaredoxin systems in the two symbiotic partners during symbiosis. The crucial role of glutathione in redox balance and S-metabolism is presented. We also highlight the specific role of some thioredoxin and glutaredoxin systems in bacterial differentiation. Transcriptomics data concerning genes encoding components and targets of thioredoxin and glutaredoxin systems in connection with the developmental step of the nodule are also considered in the model system Medicago truncatula–Sinorhizobium meliloti.
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Chaulagain, Diptee, and Julia Frugoli. "The Regulation of Nodule Number in Legumes Is a Balance of Three Signal Transduction Pathways." International Journal of Molecular Sciences 22, no. 3 (January 23, 2021): 1117. http://dx.doi.org/10.3390/ijms22031117.
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Nitrogen is a major determinant of plant growth and productivity and the ability of legumes to form a symbiotic relationship with nitrogen-fixing rhizobia bacteria allows legumes to exploit nitrogen-poor niches in the biosphere. But hosting nitrogen-fixing bacteria comes with a metabolic cost, and the process requires regulation. The symbiosis is regulated through three signal transduction pathways: in response to available nitrogen, at the initiation of contact between the organisms, and during the development of the nodules that will host the rhizobia. Here we provide an overview of our knowledge of how the three signaling pathways operate in space and time, and what we know about the cross-talk between symbiotic signaling for nodule initiation and organogenesis, nitrate dependent signaling, and autoregulation of nodulation. Identification of common components and points of intersection suggest directions for research on the fine-tuning of the plant’s response to rhizobia.
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Bonaldi, Katia, Benjamin Gourion, Joel Fardoux, Laure Hannibal, Fabienne Cartieaux, Marc Boursot, David Vallenet, et al. "Large-Scale Transposon Mutagenesis of Photosynthetic Bradyrhizobium Sp. Strain ORS278 Reveals New Genetic Loci Putatively Important for Nod-Independent Symbiosis with Aeschynomene indica." Molecular Plant-Microbe Interactions® 23, no. 6 (June 2010): 760–70. http://dx.doi.org/10.1094/mpmi-23-6-0760.
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Photosynthetic Bradyrhizobium strains possess the unusual ability to form nitrogen-fixing nodules on a specific group of legumes in the absence of Nod factors. To obtain insight into the bacterial genes involved in this Nod-independent symbiosis, we screened 15,648 Tn5 mutants of Bradyrhizobium sp. strain ORS278 for clones affected in root symbiosis with Aeschynomene indica. From the 268 isolated mutants, 120 mutants were altered in nodule development (Ndv–) and 148 mutants were found to be deficient in nitrogen fixation (Fix–). More than 50% of the Ndv– mutants were found to be altered in purine biosynthesis, strengthening the previous hypothesis of a symbiotic role of a bacterial purine derivative during the Nod-independent symbiosis. The other Ndv– mutants were auxotrophic for pyrimidines and amino acids (leucine, glutamate, and lysine) or impaired in genes encoding proteins of unknown function. The Fix– mutants were found to be affected in a wide variety of cellular processes, including both novel (n = 56) and previously identified (n = 31) genes important in symbiosis. Among the novel genes identified, several were involved in the Calvin cycle, suggesting that CO2 fixation could play an important role during this symbiosis.
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Kinkema, Mark, Paul T. Scott, and Peter M. Gresshoff. "Legume nodulation: successful symbiosis through short- and long-distance signalling." Functional Plant Biology 33, no. 8 (2006): 707. http://dx.doi.org/10.1071/fp06056.
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Nodulation in legumes provides a major conduit of available nitrogen into the biosphere. The development of nitrogen-fixing nodules results from a symbiotic interaction between soil bacteria, commonly called rhizobia, and legume plants. Molecular genetic analysis in both model and agriculturally important legume species has resulted in the identification of a variety of genes that are essential for the establishment, maintenance and regulation of this symbiosis. Autoregulation of nodulation (AON) is a major internal process by which nodule numbers are controlled through prior nodulation events. Characterisation of AON-deficient mutants has revealed a novel systemic signal transduction pathway controlled by a receptor-like kinase. This review reports our present level of understanding on the short- and long-distance signalling networks controlling early nodulation events and AON.
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Berger, Antoine, Alexandre Boscari, Pierre Frendo, and Renaud Brouquisse. "Nitric oxide signaling, metabolism and toxicity in nitrogen-fixing symbiosis." Journal of Experimental Botany 70, no. 17 (April 10, 2019): 4505–20. http://dx.doi.org/10.1093/jxb/erz159.
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AbstractInteractions between legumes and rhizobia lead to the establishment of a symbiotic relationship characterized by the formation of a new organ, the nodule, which facilitates the fixation of atmospheric nitrogen (N2) by nitrogenase through the creation of a hypoxic environment. Significant amounts of nitric oxide (NO) accumulate at different stages of nodule development, suggesting that NO performs specific signaling and/or metabolic functions during symbiosis. NO, which regulates nodule gene expression, accumulates to high levels in hypoxic nodules. NO accumulation is considered to assist energy metabolism within the hypoxic environment of the nodule via a phytoglobin–NO-mediated respiration process. NO is a potent inhibitor of the activity of nitrogenase and other plant and bacterial enzymes, acting as a developmental signal in the induction of nodule senescence. Hence, key questions concern the relative importance of the signaling and metabolic functions of NO versus its toxic action and how NO levels are regulated to be compatible with nitrogen fixation functions. This review analyses these paradoxical roles of NO at various stages of symbiosis, and highlights the role of plant phytoglobins and bacterial hemoproteins in the control of NO accumulation.
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Uchiumi, Toshiki, Takuji Ohwada, Manabu Itakura, Hisayuki Mitsui, Noriyuki Nukui, Pramod Dawadi, Takakazu Kaneko, et al. "Expression Islands Clustered on the Symbiosis Island of the Mesorhizobium loti Genome." Journal of Bacteriology 186, no. 8 (April 15, 2004): 2439–48. http://dx.doi.org/10.1128/jb.186.8.2439-2448.2004.
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ABSTRACT Rhizobia are symbiotic nitrogen-fixing soil bacteria that are associated with host legumes. The establishment of rhizobial symbiosis requires signal exchanges between partners in microaerobic environments that result in mutualism for the two partners. We developed a macroarray for Mesorhizobium loti MAFF303099, a microsymbiont of the model legume Lotus japonicus, and monitored the transcriptional dynamics of the bacterium during symbiosis, microaerobiosis, and starvation. Global transcriptional profiling demonstrated that the clusters of genes within the symbiosis island (611 kb), a transmissible region distinct from other chromosomal regions, are collectively expressed during symbiosis, whereas genes outside the island are downregulated. This finding implies that the huge symbiosis island functions as clustered expression islands to support symbiotic nitrogen fixation. Interestingly, most transposase genes on the symbiosis island were highly upregulated in bacteroids, as were nif, fix, fdx, and rpoN. The genome region containing the fixNOPQ genes outside the symbiosis island was markedly upregulated as another expression island under both microaerobic and symbiotic conditions. The symbiosis profiling data suggested that there was activation of amino acid metabolism, as well as nif-fix gene expression. In contrast, genes for cell wall synthesis, cell division, DNA replication, and flagella were strongly repressed in differentiated bacteroids. A highly upregulated gene in bacteroids, mlr5932 (encoding 1-aminocyclopropane-1-carboxylate deaminase), was disrupted and was confirmed to be involved in nodulation enhancement, indicating that disruption of highly expressed genes is a useful strategy for exploring novel gene functions in symbiosis.
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Hoang, Nhung T., Katalin Tóth, and Gary Stacey. "The role of microRNAs in the legume–Rhizobium nitrogen-fixing symbiosis." Journal of Experimental Botany 71, no. 5 (March 12, 2020): 1668–80. http://dx.doi.org/10.1093/jxb/eraa018.
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Abstract Under nitrogen starvation, most legume plants form a nitrogen-fixing symbiosis with Rhizobium bacteria. The bacteria induce the formation of a novel organ called the nodule in which rhizobia reside as intracellular symbionts and convert atmospheric nitrogen into ammonia. During this symbiosis, miRNAs are essential for coordinating the various plant processes required for nodule formation and function. miRNAs are non-coding, endogenous RNA molecules, typically 20–24 nucleotides long, that negatively regulate the expression of their target mRNAs. Some miRNAs can move systemically within plant tissues through the vascular system, which mediates, for example, communication between the stem/leaf tissues and the roots. In this review, we summarize the growing number of miRNAs that function during legume nodulation focusing on two model legumes, Lotus japonicus and Medicago truncatula, and two important legume crops, soybean (Glycine max) and common bean (Phaseolus vulgaris). This regulation impacts a variety of physiological processes including hormone signaling and spatial regulation of gene expression. The role of mobile miRNAs in regulating legume nodule number is also highlighted.
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Prévost, Danielle, Pascal Drouin, Serge Laberge, Annick Bertrand, Jean Cloutier, and Gabriel Lévesque. "Cold-adapted rhizobia for nitrogen fixation in temperate regions." Canadian Journal of Botany 81, no. 12 (December 1, 2003): 1153–61. http://dx.doi.org/10.1139/b03-113.
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Rhizobia from Canadian soils were selected for cold adaptation with the aim of improving productivity of legumes that are subjected to cool temperatures during the growing season. One approach was to use rhizobia associated with legume species indigenous to arctic and subarctic regions: (i) Mesorhizobium sp. isolated from Astragalus and Oxytropis spp. and (ii) Rhizobium leguminosarum from Lathryrus spp. The majority of these rhizobia are considered psychrotrophs because they can grow at 0 °C. The advantages of cold adaptation of arctic Mesorhizobium to improve legume symbiosis were demonstrated with the temperate forage legume sainfoin (Onobrychis viciifolia). In laboratory and field studies, arctic rhizobia were more efficient than temperate (commercial) rhizobia in improving growth of sainfoin and were more competitive in forming nodules. Biochemical studies on cold adaptation showed higher synthesis of cold shock proteins in cold-adapted than in nonadapted arctic rhizobia. Since arctic Mesorhizobium cannot nodulate agronomically important legumes, the nodulation genes and the bacterial signals (Nod factors) were characterized as a first step to modifying the host specificity of nodulation. Another valuable approach was to screen for cold adaptation, that is, rhizobia naturally associated with agronomic legumes cultivated in temperate areas. A superior strain of Sinorhizobium meliloti adapted for nodulation of alfalfa at low temperatures was selected and was the most efficient for improving growth of alfalfa in laboratory and field studies. This strain also performed well in improving regrowth of alfalfa after overwintering under cold and anaerobic (ice encasement) stresses, indicating a possible cross-adaptation of selected rhizobia for various abiotic stresses inherent to temperate climates.Key words: cold adaptation, legumes, symbiotic efficiency, cold shock protein, nodulation genes, anaerobiosis.
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Scheublin, Tanja R., Karyn P. Ridgway, J. Peter W. Young, and Marcel G. A. van der Heijden. "Nonlegumes, Legumes, and Root Nodules Harbor Different Arbuscular Mycorrhizal Fungal Communities." Applied and Environmental Microbiology 70, no. 10 (October 2004): 6240–46. http://dx.doi.org/10.1128/aem.70.10.6240-6246.2004.
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ABSTRACT Legumes are an important plant functional group since they can form a tripartite symbiosis with nitrogen-fixing Rhizobium bacteria and phosphorus-acquiring arbuscular mycorrhizal fungi (AMF). However, not much is known about AMF community composition in legumes and their root nodules. In this study, we analyzed the AMF community composition in the roots of three nonlegumes and in the roots and root nodules of three legumes growing in a natural dune grassland. We amplified a portion of the small-subunit ribosomal DNA and analyzed it by using restriction fragment length polymorphism and direct sequencing. We found differences in AMF communities between legumes and nonlegumes and between legume roots and root nodules. Different plant species also contained different AMF communities, with different AMF diversity. One AMF sequence type was much more abundant in legumes than in nonlegumes (39 and 13%, respectively). Root nodules contained characteristic AMF communities that were different from those in legume roots, even though the communities were similar in nodules from different legume species. One AMF sequence type was found almost exclusively in root nodules. Legumes and root nodules have relatively high nitrogen concentrations and high phosphorus demands. Accordingly, the presence of legume- and nodule-related AMF can be explained by the specific nutritional requirements of legumes or by host-specific interactions among legumes, root nodules, and AMF. In summary, we found that AMF communities vary between plant functional groups (legumes and nonlegumes), between plant species, and between parts of a root system (roots and root nodules).
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Tsikou, Daniela, Zhe Yan, Dennis B. Holt, Nikolaj B. Abel, Dugald E. Reid, Lene H. Madsen, Hemal Bhasin, Moritz Sexauer, Jens Stougaard, and Katharina Markmann. "Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA." Science 362, no. 6411 (August 30, 2018): 233–36. http://dx.doi.org/10.1126/science.aat6907.
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Nitrogen-fixing root nodules on legumes result from two developmental processes, bacterial infection and nodule organogenesis. To balance symbiosis and plant growth, legume hosts restrict nodule numbers through an inducible autoregulatory process. Here, we present a mechanism where repression of a negative regulator ensures symbiotic susceptibility of uninfected roots of the host Lotus japonicus. We show that microRNA miR2111 undergoes shoot-to-root translocation to control rhizobial infection through posttranscriptional regulation of the symbiosis suppressor TOO MUCH LOVE in roots. miR2111 maintains a susceptible default status in uninfected hosts and functions as an activator of symbiosis downstream of LOTUS HISTIDINE KINASE1–mediated cytokinin perception in roots and HYPERNODULATION ABERRANT ROOT FORMATION1, a shoot factor in autoregulation. The miR2111-TML node ensures activation of feedback regulation to balance infection and nodulation events.
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Rigg, Jessica L., Ashlea T. Webster, Deirdre M. Harvey, Susan E. Orgill, Francesca Galea, Adrian G. Dando, Damian P. Collins, et al. "Cross-host compatibility of commercial rhizobial strains for new and existing pasture legume cultivars in south-eastern Australia." Crop and Pasture Science 72, no. 9 (2021): 652. http://dx.doi.org/10.1071/cp20234.
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Perennial legumes have potential to increase pasture productivity in the high rainfall zone (600–850 mm) of south-eastern Australia through their ability to use summer rainfall and fix nitrogen (N2). Various perennial legumes are being evaluated for this environment; however, little information exists on legume–rhizobia cross-host compatibility and its consequences for biological N2 fixation. This is especially important when legumes are sown into fields with a background of competitive rhizobia such as WSM1325 or sown as a pasture mix with different host–symbiont pairs. We studied the effectiveness and cross-host compatibility of five commercial rhizobial strains for a range of pasture legumes (nine species, 18 cultivars) under controlled environment conditions, and further evaluated nodule occupancy and competitiveness of a newly established pasture (13 species, 20 cultivars) in the field, by determining nodulation and production (biomass and N2 fixation). Three of the commercial inoculant strains formed root nodules with multiple legume species; commonly however, less N2 was fixed in cases where the inoculant was not the recommended strain for the legume species. Within a legume species, cultivars could differ in their ability to form effective root nodules with multiple rhizobial strains. White clover cvv. Trophy, Haifa and Storm, strawberry clover cv. Palestine, and Talish clover cv. Permatas formed effective nodules with both TA1 and WSM1325 rhizobial strains. White clover cultivars that could not form an effective symbiosis with the common background strain WSM1325 fixed less N2. The white clover × Caucasian clover hybrid formed effective symbiosis with strain TA1 but not with other commercial strains. Some species such as birdsfoot trefoil, Talish clover, sulfur clover and tetraploid Caucasian clover formed ineffective symbiosis in the field. Until resolved, this will likely inhibit their further development as pasture plants for similar permanent pasture environments.
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Staehelin, Christian, Lennart S. Forsberg, Wim D'Haeze, Mu-Yun Gao, Russell W. Carlson, Zhi-Ping Xie, Brett J. Pellock, et al. "Exo-Oligosaccharides of Rhizobium sp. Strain NGR234 Are Required for Symbiosis with Various Legumes." Journal of Bacteriology 188, no. 17 (September 1, 2006): 6168–78. http://dx.doi.org/10.1128/jb.00365-06.
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ABSTRACT Rhizobia are nitrogen-fixing bacteria that establish endosymbiotic associations with legumes. Nodule formation depends on various bacterial carbohydrates, including lipopolysaccharides, K-antigens, and exopolysaccharides (EPS). An acidic EPS from Rhizobium sp. strain NGR234 consists of glucosyl (Glc), galactosyl (Gal), glucuronosyl (GlcA), and 4,6-pyruvylated galactosyl (PvGal) residues with β-1,3, β-1,4, β-1,6, α-1,3, and α-1,4 glycoside linkages. Here we examined the role of NGR234 genes in the synthesis of EPS. Deletions within the exoF, exoL, exoP, exoQ, and exoY genes suppressed accumulation of EPS in bacterial supernatants, a finding that was confirmed by chemical analyses. The data suggest that the repeating subunits of EPS are assembled by an ExoQ/ExoP/ExoF-dependent mechanism, which is related to the Wzy polymerization system of group 1 capsular polysaccharides in Escherichia coli. Mutation of exoK (NGRΩexoK), which encodes a putative glycanase, resulted in the absence of low-molecular-weight forms of EPS. Analysis of the extracellular carbohydrates revealed that NGRΩexoK is unable to accumulate exo-oligosaccharides (EOSs), which are O-acetylated nonasaccharide subunits of EPS having the formula Gal(Glc)5(GlcA)2PvGal. When used as inoculants, both the exo-deficient mutants and NGRΩexoK were unable to form nitrogen-fixing nodules on some hosts (e.g., Albizia lebbeck and Leucaena leucocephala), but they were able to form nitrogen-fixing nodules on other hosts (e.g., Vigna unguiculata). EOSs of the parent strain were biologically active at very low levels (yield in culture supernatants, ∼50 μg per liter). Thus, NGR234 produces symbiotically active EOSs by enzymatic degradation of EPS, using the extracellular endo-β-1,4-glycanase encoded by exoK (glycoside hydrolase family 16). We propose that the derived EOSs (and not EPS) are bacterial components that play a crucial role in nodule formation in various legumes.
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Ruiz, Bryan, Åsa Frostegård, Claude Bruand, and Eliane Meilhoc. "Rhizobia: highways to NO." Biochemical Society Transactions 49, no. 1 (February 5, 2021): 495–505. http://dx.doi.org/10.1042/bst20200989.
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The interaction between rhizobia and their legume host plants conduces to the formation of specialized root organs called nodules where rhizobia differentiate into bacteroids which fix atmospheric nitrogen to the benefit of the plant. This beneficial symbiosis is of importance in the context of sustainable agriculture as legumes do not require the addition of nitrogen fertilizer to grow. Interestingly, nitric oxide (NO) has been detected at various steps of the rhizobium–legume symbiosis where it has been shown to play multifaceted roles. Both bacterial and plant partners are involved in NO synthesis in nodules. To better understand the role of NO, and in particular the role of bacterial NO, at all steps of rhizobia–legumes interaction, the enzymatic sources of NO have to be elucidated. In this review, we discuss different enzymatic reactions by which rhizobia may potentially produce NO. We argue that there is most probably no NO synthase activity in rhizobia, and that instead the NO2− reductase nirK, which is part of the denitrification pathway, is the main bacterial source of NO. The nitrate assimilation pathway might contribute to NO production but only when denitrification is active. The different approaches to measure NO in rhizobia are also addressed.
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Messinese, Elsa, Jeong-Hwan Mun, Li Huey Yeun, Dhileepkumar Jayaraman, Pierre Rougé, Annick Barre, Géraldine Lougnon, et al. "A Novel Nuclear Protein Interacts With the Symbiotic DMI3 Calcium- and Calmodulin-Dependent Protein Kinase of Medicago truncatula." Molecular Plant-Microbe Interactions® 20, no. 8 (August 2007): 912–21. http://dx.doi.org/10.1094/mpmi-20-8-0912.
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Many higher plants establish symbiotic relationships with arbuscular mycorrhizal (AM) fungi that improve their ability to acquire nutrients from the soil. In addition to establishing AM symbiosis, legumes also enter into a nitrogen-fixing symbiosis with bacteria known as rhizobia that results in the formation of root nodules. Several genes involved in the perception and transduction of bacterial symbiotic signals named “Nod factors” have been cloned recently in model legumes through forward genetic approaches. Among them, DMI3(Doesn't Make Infections 3) is a calcium- and calmodulin-dependent kinase required for the establishment of both nodulation and AM symbiosis. We have identified, by a yeast two-hybrid system, a novel protein interacting with DMI3 named IPD3 (Interacting Protein of DMI3). IPD3 is predicted to interact with DMI3 through a C-terminal coiled-coil domain. Chimeric IPD3∷GFP is localized to the nucleus of transformed Medicago truncatula root cells, in which split yellow fluorescent protein assays suggest that IPD3 and DMI3 physically interact in Nicotiana benthamiana. Like DMI3, IPD3 is extremely well conserved among the angiosperms and is absent from Arabidopsis. Despite this high level of conservation, none of the homologous proteins have a demonstrated biological or biochemical function. This work provides the first evidence of the involvement of IPD3 in a nuclear interaction with DMI3.
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Arrighi, Jean-François, Fabienne Cartieaux, Spencer C. Brown, Marguerite Rodier-Goud, Marc Boursot, Joel Fardoux, Delphine Patrel, et al. "Aeschynomene evenia, a Model Plant for Studying the Molecular Genetics of the Nod-Independent Rhizobium-Legume Symbiosis." Molecular Plant-Microbe Interactions® 25, no. 7 (July 2012): 851–61. http://dx.doi.org/10.1094/mpmi-02-12-0045-ta.
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Research on the nitrogen-fixing symbiosis has been focused, thus far, on two model legumes, Medicago truncatula and Lotus japonicus, which use a sophisticated infection process involving infection thread formation. However, in 25% of the legumes, the bacterial entry occurs more simply in an intercellular fashion. Among them, some Aeschynomene spp. are nodulated by photosynthetic Bradyrhizobium spp. that do not produce Nod factors. This interaction is believed to represent a living testimony of the ancestral state of the rhizobium–legume symbiosis. To decipher the mechanisms of this Nod-independent process, we propose Aeschynomene evenia as a model legume because it presents all the characteristics required for genetic and molecular analysis. It is a short-perennial and autogamous species, with a diploid and relatively small genome (2n = 20; 460 Mb/1C). A. evenia ‘IRFL6945’ is nodulated by the well-characterized photosynthetic Bradyrhizobium sp. strain ORS278 and is efficiently transformed by Agrobacterium rhizogenes. Aeschynomene evenia is genetically homozygous but polymorphic accessions were found. A manual hybridization procedure has been set up, allowing directed crosses. Therefore, it should be relatively straightforward to unravel the molecular determinants of the Nod-independent process in A. evenia. This should shed new light on the evolution of rhizobium–legume symbiosis and could have important agronomic implications.
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Schrader, James A., Mark Kroggel, and William R. Graves. "Nodulation and Nitrogen-fixing Capacity of Rhizobial Isolates from China in Symbiosis with Maackia amurensis." Journal of Environmental Horticulture 25, no. 1 (March 1, 2007): 47–50. http://dx.doi.org/10.24266/0738-2898-25.1.47.
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Abstract Maackia amurensis Rupr. & Maxim (Amur maackia) is a leguminous Asian tree capable of forming N2-fixing symbioses with soil-borne Bradyrhizobium spp. This trait sets Amur maackia apart from many legumes now produced in North American nurseries. Two determinants of N2-fixing capacity in legumes are the compatibility of the host plant and its bacterial microsymbiont and the metabolic efficiency of compatible bacteria. Our objectives were to isolate numerous rhizobia from the root zones of indigenous Amur maackia in China and to select isolates that form superior N2-fixing relationships with inoculated seedlings. Soil samples collected in the Heilongjiang Province of China were used as inocula to establish nodules on seedlings. Putative rhizobia were isolated from these nodules and cultured. Inoculation of additional seedlings with 170 of these isolates evoked nodulation, confirming their identity as rhizobia. Isolates that induced the most nodules were evaluated further. All selected isolates increased growth and total N content of Amur maackia compared to uninoculated controls. Three of the isolates induced more root nodules, and four evoked a higher total N content in plants than did isolate USDA 4349, a previously characterized strain of Bradyrhizobium selected for Amur maackia. Our results demonstrate marked variation among rhizobia compatible with Amur maackia and illustrate the potential to inoculate plants in nurseries and landscapes with superior bacteria, a practice that could reduce fertilizer use and improve performance of trees in N-deficient soils.
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Pawlowski, Katharina, Susan Swensen, Changhui Guan, Az-Eddine Hadri, Alison M. Berry, and Ton Bisseling. "Distinct Patterns of Symbiosis-Related Gene Expression in Actinorhizal Nodules from Different Plant Families." Molecular Plant-Microbe Interactions® 16, no. 9 (September 2003): 796–807. http://dx.doi.org/10.1094/mpmi.2003.16.9.796.
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Phylogenetic analyses suggest that, among the members of the Eurosid I clade, nitrogen-fixing root nodule symbioses developed multiple times independently, four times with rhizobia and four times with the genus Frankia. In order to understand the degree of similarity between symbiotic systems of different phylogenetic subgroups, gene expression patterns were analyzed in root nodules of Datisca glomerata and compared with those in nodules of another actinorhizal plant, Alnus glutinosa, and with the expression patterns of homologous genes in legumes. In parallel, the phylogeny of actinorhizal plants was examined more closely. The results suggest that, although relationships between major groups are difficult to resolve using molecular phylogenetic analysis, the comparison of gene expression patterns can be used to inform evolutionary relationships. In this case, stronger similarities were found between legumes and intracellularly infected actinorhizal plants (Alnus) than between actinorhizal plants of two different phylogenetic subgroups (Alnus/Datisca).
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Ballard, R. A., and N. Charman. "Nodulation and growth of pasture legumes with naturalised soil rhizobia. 1. Annual Medicago spp." Australian Journal of Experimental Agriculture 40, no. 7 (2000): 939. http://dx.doi.org/10.1071/ea99112.
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The ability of 11 species of annual medics (Medicago doliata, M. laciniata, M. littoralis, M. minima, M. orbicularis, M. polymorpha, M. praecox, M. rigidula, M. rigiduloides, M. tornata and M. truncatula) to nodulate and fix nitrogen with naturalised rhizobia from 28 South Australian soils was assessed. The number of rhizobia in the soils was estimated. Medic shoot dry matter production and nodulation were measured, after inoculation of medic seedlings with a soil suspension, in 2 glasshouse experiments. The number of medic rhizobia ranged from 0.4 10 2 to 1.5 10 6 per gram soil. Medicago laciniata was the only medic species tested which was not consistently nodulated by the soil rhizobia. While all the other species formed nodules, they varied widely in their ability to form an effective symbiosis. Symbiotic performance (which indicates how much growth the medic line achieved, when compared to an effective inoculation treatment) of the medic species ranged from 3% (M. rigiduloides) to 67% (M. praecox). Herald (M. littoralis) achieved a symbiotic performance of 49% and it was estimated that this would be insufficient to meet the nitrogen requirements of a Herald-based pasture during early growth. The symbiotic performance of Santiago (M. polymorpha) was low (17%) and erratic (from –6 to 72%). The ability of the rhizobia to form an effective symbiosis varied widely also between soil regions. For example, the rhizobia in Riverland soils resulted in only 31% of the shoot dry matter of those in Eyre Peninsula soils, in association with M. polymorpha. There are significant opportunities to improve the symbiotic performance of a number of the species of annual medics examined in this study. Options to improve the effectiveness of the symbiosis of medics with naturalised soil rhizobia are discussed.
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Gully, Djamel, Daniel Gargani, Katia Bonaldi, Cédric Grangeteau, Clémence Chaintreuil, Joël Fardoux, Phuong Nguyen, et al. "A Peptidoglycan-Remodeling Enzyme Is Critical for Bacteroid Differentiation in Bradyrhizobium spp. During Legume Symbiosis." Molecular Plant-Microbe Interactions® 29, no. 6 (June 2016): 447–57. http://dx.doi.org/10.1094/mpmi-03-16-0052-r.
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In response to the presence of compatible rhizobium bacteria, legumes form symbiotic organs called nodules on their roots. These nodules house nitrogen-fixing bacteroids that are a differentiated form of the rhizobium bacteria. In some legumes, the bacteroid differentiation comprises a dramatic cell enlargement, polyploidization, and other morphological changes. Here, we demonstrate that a peptidoglycan-modifying enzyme in Bradyrhizobium strains, a DD-carboxypeptidase that contains a peptidoglycan-binding SPOR domain, is essential for normal bacteroid differentiation in Aeschynomene species. The corresponding mutants formed bacteroids that are malformed and hypertrophied. However, in soybean, a plant that does not induce morphological differentiation of its symbiont, the mutation does not affect the bacteroids. Remarkably, the mutation also leads to necrosis in a large fraction of the Aeschynomene nodules, indicating that a normally formed peptidoglycan layer is essential for avoiding the induction of plant immune responses by the invading bacteria. In addition to exopolysaccharides, capsular polysaccharides, and lipopolysaccharides, whose role during symbiosis is well defined, our work demonstrates an essential role in symbiosis for yet another rhizobial envelope component, the peptidoglycan layer.
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Dantas, Edilândia Farias, Ana Dolores Santiago de Freitas, Maria do Carmo Catanho Pereira de Lyra, Carolina Etienne de Rosália e. Silva Santos, Stella Jorge de Carvalho Neta, Augusto Cesar de Arruda Santana, Rosemberg de Vasconcelos Bezerra, and Everardo Valadares de Sá Barretto Sampaio. "Biological fixation, transfer and balance of nitrogen in passion fruit (Passiflora edulis Sims) orchard intercropped with different green manure crops." 2019 13, (03) 2019 (March 20, 2019): 465–71. http://dx.doi.org/10.21475/ajcs.19.13.03.p1559.
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Green manures can replace or supplement mineral fertilization and add organic matter to the soils, ensuring greater sustainability to fruit growing in semiarid regions. Biological fixation, transfer and balance of nitrogen were determined on an irrigated yellow passion fruit orchard (Passiflora edulis Sims) intercropped separately with three cover crops: sunn hemp, Crotalaria juncea (L.); pigeon pea, Cajanus cajan (L.) Mill; and jack bean, Canavalia ensiformis (L.) DC. In a fourth treatment, legumes were not planted, but spontaneous vegetation was left to grow freely. The legumes were croped for 90 days in three lines (0.5 m apart) inside the passion fruit plant lines (2.5 m apart). Fixation and transfers were determined by the 15N natural abundance technique, using sunflower as a reference plant. The three planted legumes nodulated abundantly and fixed nitrogen in high proportions (between 50 and 90% of their N), forming symbiosis with bacteria naturally established in the soil. Jack bean produced more biomass than sunn hemp and pigeon pea, and as much as the spontaneous plants, of which 23% were legumes. The amounts of fixed N (150, 43, 30 and 29 kg ha-1) were determined mainly by the biomass of legumes. More than 40% of the N of passion fruit plants came from the biological nitrogen fixation of the intercropped jack bean, which provided an amount of N higher than that exported in the fruits, generating a positive balance of more than 100 kg ha-1. Therefore, it is recommended to intercrop jack bean in irrigated passion fruit orchards.
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Regus, John U., Kelsey A. Gano, Amanda C. Hollowell, and Joel L. Sachs. "Efficiency of partner choice and sanctions in Lotus is not altered by nitrogen fertilization." Proceedings of the Royal Society B: Biological Sciences 281, no. 1781 (April 22, 2014): 20132587. http://dx.doi.org/10.1098/rspb.2013.2587.
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Eukaryotic hosts must exhibit control mechanisms to select against ineffective bacterial symbionts. Hosts can minimize infection by less-effective symbionts (partner choice) and can divest of uncooperative bacteria after infection (sanctions). Yet, such host-control traits are predicted to be context dependent, especially if they are costly for hosts to express or maintain. Legumes form symbiosis with rhizobia that vary in symbiotic effectiveness (nitrogen fixation) and can enforce partner choice as well as sanctions. In nature, legumes acquire fixed nitrogen from both rhizobia and soils, and nitrogen deposition is rapidly enriching soils globally. If soil nitrogen is abundant, we predict host control to be downregulated, potentially allowing invasion of ineffective symbionts. We experimentally manipulated soil nitrogen to examine context dependence in host control. We co-inoculated Lotus strigosus from nitrogen depauperate soils with pairs of Bradyrhizobium strains that vary in symbiotic effectiveness and fertilized plants with either zero nitrogen or growth maximizing nitrogen. We found efficient partner choice and sanctions regardless of nitrogen fertilization, symbiotic partner combination or growth season. Strikingly, host control was efficient even when L. strigosus gained no significant benefit from rhizobial infection, suggesting that these traits are resilient to short-term changes in extrinsic nitrogen, whether natural or anthropogenic.
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Dolgikh, Alexandra V., Elizaveta S. Rudaya, and Elena A. Dolgikh. "Identification of BELL Transcription Factors Involved in Nodule Initiation and Development in the Legumes Pisum sativum and Medicago truncatula." Plants 9, no. 12 (December 20, 2020): 1808. http://dx.doi.org/10.3390/plants9121808.
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Single three-amino acid loop extension (TALE) homeodomain proteins, including the KNOTTED-like (KNOX) and BEL-like (BELL) families in plants, usually work as heterodimeric transcription factor complexes to regulate different developmental processes, often via effects on phytohormonal pathways. Nitrogen-fixing nodule formation in legumes is regulated by different families of homeodomain transcription factors. Whereas the role of KNOX transcription factors in the control of symbiosis was studied early, BELL transcription factors have received less attention. Here, we report the identification and expression analysis of BELL genes in the legume plants Medicago truncatula and Pisum sativum, which are involved in regulating symbiosis initiation and development. A more precise analysis was performed for the most significantly upregulated PsBELL1-2 gene in pea. We found that the PsBELL1-2 transcription factor could be a potential partner of PsKNOX9. In addition, we showed that PsBELL1-2 can interact with the PsDELLA1 (LA) protein-regulator of the gibberellin pathway, which has a previously demonstrated important role in symbiosis development.
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van Velzen, Robin, Rens Holmer, Fengjiao Bu, Luuk Rutten, Arjan van Zeijl, Wei Liu, Luca Santuari, et al. "Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses." Proceedings of the National Academy of Sciences 115, no. 20 (May 1, 2018): E4700—E4709. http://dx.doi.org/10.1073/pnas.1721395115.
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Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.